Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase

EMBO Journal

Volumn 28, Issue 12, 2009, Pages 1803-1811

  Sugiyama, Kanako ^a   Obayashi, Eiji ^a   Kawaguchi, Atsushi ^b   Suzuki, Yukari ^b   Tame, Jeremy R H ^a   Nagata, Kyosuke ^b   Park, Sam Yong ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Influenza virus; Interface; Mutant; RNA polymerase; Structure

Indexed keywords

CAP BINDING PROTEIN; ENDONUCLEASE; GENOMIC RNA; OLIGONUCLEOTIDE; RNA; RNA BINDING PROTEIN; RNA POLYMERASE; RNA POLYMERASE PB1 SUBUNIT; RNA POLYMERASE PB2 SUBUNIT; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS MESSENGER RNA; DNA DIRECTED RNA POLYMERASE; PROTEIN SUBUNIT; VALINE; VIRUS RNA;

ANIMAL CELL; ARTICLE; BINDING ASSAY; CELL STRAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME SUBUNIT; GENE EXPRESSION; GENETIC TRANSFECTION; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SYNTHESIS; SIGNAL TRANSDUCTION; VIRUS RECOMBINANT; X RAY DIFFRACTION; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DOG; ENZYMOLOGY; GENETICS; INFLUENZA VIRUS A H1N1; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY;

AVES; HUMAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DNA-DIRECTED RNA POLYMERASES; DOGS; INFLUENZA A VIRUS, H1N1 SUBTYPE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RNA, VIRAL; STATIC ELECTRICITY; VALINE;

EID: 67649552964     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.138     Document Type: Article

References (48)

1. Barcena J, Ochoa M, de la Luna S, Melero JA, Nieto A, Ortin J,
2. Portela A (1994) Monoclonal antibodies against influenza virus PB2 and NP polypeptides interfere with the initiation step of viral mRNA synthesis in vitro. J Virol 68: 6900-6909
3. Biswas SK, Nayak DP (1996) Influenza virus polymerase basic protein 1 interacts with influenza virus polymerase basic protein 2 at multiple sites. J Virol 70: 6716-6722
4. Cianci C, Tiley L, Krystal M (1995) Differential activation of the influenza virus polymerase via template RNA binding. J Virol 69: 3995-3999 Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F,
5. Cusack S, Ruigrok RW (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458: 914-918
6. Digard P, Blok VC, Inglis SC (1989) Complex formation between influenza virus polymerase proteins expressed in Xenopus oocytes. Virology 171: 162-169
7. Elton D, Digard P, Tiley L, Ortin J (2005) Structure and function of the influenza virus RNP. In Current Topics in Influenza Virology, Kawaoka Y (ed), pp 1-92. Norfolk: Horizon Scientific Press
8. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132
9. Fodor E, Crow M, Mingay LJ, Deng T, Sharps J, Fechter P, Brownlee GG (2002) A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J Virol 76: 8989-9001
10. Gonzalez S, Zurcher T, Ortin J (1996) Identification of two separate domains in the influenza virus PB1 protein involved in the interaction with the PB2 and PA subunits: a model for the viral RNA polymerase structure. Nucleic Acids Res 24: 4456-4463
11. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, Lewis J, Ruigrok RW, Ortin J, Hart DJ, Cusack S (2008) The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15: 500-506
12. Hara K, Schmidt FI, Crow M, Brownlee GG (2006) Amino acid residues in the N-terminal region of the PA subunit of influenza A virus RNA polymerase play a critical role in protein stability, endonuclease activity, cap binding, and virion RNA promoter binding. J Virol 80: 7789-7798
13. He X, Zhou J, Bartlam M, Zhang R, Ma J, Lou Z, Li X, Li J, Joachimiak A, Zeng Z, Ge R, Rao Z, Liu Y (2008) Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454: 1123-1126
14. Huang TS, Palese P, Krystal M (1990) Determination of influenza virus proteins required for genome replication. J Virol 64: 5669-5673
15. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797
16. Laskowski RA, Moss DS, Thornton JM (1993) Main-chain bond lengths and bond angles in protein structures. J Mol Biol 231: 1049-1067
17. Li ML, Ramirez BC, Krug RM (1998) RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding sites. EMBO J 17: 5844-5852
18. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255
19. Nagata K, Kawaguchi A, Naito T (2008) Host factors for replication and transcription of the influenza virus genome. Rev Med Virol 18: 247-260
20. Neumann G,Watanabe T, Ito H,Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y (1999) Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA 96: 9345-9350
21. Obayashi E, Yoshida H, Kawai F, Shibayama N, Kawaguchi A, Nagata K, Tame JR, Park SY (2008) The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 454: 1127-1131
22. Ochoa M, Barcena J, de la Luna S, Melero JA, Douglas AR, Nieto A, Ortin J, Skehel JJ, Portela A (1995) Epitope mapping of crossreactive monoclonal antibodies specific for the influenza A virus PA and PB2 polypeptides. Virus Res 37: 305-315
23. Ohtsu Y, Honda Y, Sakata Y, Kato H, Toyoda T (2002) Fine mapping of the subunit binding sites of influenza virus RNA polymerase. Microbiol Immunol 46: 167-175
24. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
25. Peiris JS, de Jong MD, Guan Y (2007) Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20: 243-267
26. Perales B, de la Luna S, Palacios I, Ortin J (1996) Mutational analysis identifies functional domains in the influenza A virus PB2 polymerase subunit. J Virol 70: 1678-1686
27. Plotch SJ, Bouloy M, Ulmanen I, Krug RM (1981) A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23: 847-858
28. Poole E, Elton D, Medcalf L, Digard P (2004) Functional domains of the influenza A virus PB2 protein: identification of NP- and PB1-binding sites. Virology 321: 120-133
29. Poole EL, Medcalf L, Elton D, Digard P (2007) Evidence that the Cterminal PB2-binding region of the influenza A virus PB1 protein is a discrete alpha-helical domain. FEBS Lett 581: 5300-5306
30. Poon LL, Pritlove DC, Fodor E, Brownlee GG (1999) Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. J Virol 73: 3473-3476
31. Portela A, Digard P (2002) The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 83: 723-734
32. Sheldrick GM (1986) SHELXS86-Program for Crystal Structure Solution. Germany: University of Gottingen
33. St Angelo C, Smith GE, Summers MD, Krug RM (1987) Two of the three influenza viral polymerase proteins expressed by using baculovirus vectors form a complex in insect cells. J Virol 61: 361-365
34. Tarendeau F, Boudet J, Guilligay D, Mas PJ, Bougault CM, Boulo S, Baudin F, Ruigrok RW, Daigle N, Ellenberg J, Cusack S, Simorre JP, Hart DJ (2007) Structure and nuclear import function of the Cterminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14: 229-233
35. Tarendeau F, Crepin T, Guilligay D, Ruigrok RW, Cusack S, Hart DJ (2008) Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 4: e1000136
36. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG
37. Characterization of the 1918 influenza virus polymerase genes. Nature 437: 889-893
38. Terwilliger TC (2003) SOLVE and RESOLVE: automated structure solution and density modification. Methods Enzymol 374: 22-37
39. Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55: 849-861
40. Toyoda T, Adyshev DM, Kobayashi M, Iwata A, Ishihama A (1996) Molecular assembly of the influenza virus RNA polymerase: determination of the subunit-subunit contact sites. J Gen Virol 77(Part 9): 2149-2157
41. Treanor J, Perkins M, Battaglia R, Murphy BR (1994) Evaluation of the genetic stability of the temperature-sensitive PB2 gene mutation of the influenza A/Ann Arbor/6/60 cold-adapted vaccine virus. J Virol 68: 7684-7688
42. Vreede FT, Jung TE, Brownlee GG (2004) Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J Virol 78: 9568-9572
43. Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8: 127-134
44. Whittaker GR, Digard P (2005) Entry and intercellular transport of influenza virus. In Current Topics in Influenza Virology, Kawaoka Y (ed), pp 37-64. Norfolk: Horizon Scientific Press
45. World Health Organization (WHO) (2003) Influenza fact sheet. /http://www.who.int/mediacentre/factsheets/2003/fs211/en/S
46. Yin YW, Steitz TA (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase. Science 298: 1387-1395
47. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Lv Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458: 909-913
48. Zheng H, Lee HA, Palese P, Garcia-Sastre A (1999) Influenza A virus RNA polymerase has the ability to stutter at the polyadenylation site of a viral RNA template during RNA replication. J Virol 73: 5240-5243